Discussion
Within seven months from its start, our tick monitoring citizen science research succeeded to reveal the emergence of two adult Hyalommatick species in two different locations of Hungary. Our project highlights the importance of public relations in the success of a citizen science project. We could reach relatively high visibility (over 31000 individual website visitors) within seven months (data from Google Analytics not shown). The highest number of daily visitors, 5453 could be reached after an extensive media release of our project. Participating civilians also benefit from initiatives that use citizen science. First, in the optimal case, all such research is intended to serve the interests of society directly or indirectly, so the interest of civilian researchers is the success of the program. In addition, the increased social awareness caused by various citizen science projects is a positive side effect. Due to their involvement in the survey, participants pay more attention to nature and to monitoring non-endemic tick species in their environment and the relationship between participating citizens, scientists and public health agencies may also become closer. Our participants received reply from us regarding their questions and samples within 24 hours. This was important because some secondary media appearances, emphasizing the seriousness of Crimean-Congo haemorrhagic fever, were frightening some of our responders, and in most of the cases they were comforted by the fact that the specimen they found was not a Hyalomma tick.
In addition to the advantages, we must not forget about the limitations and disadvantages of the method. For example, at the beginning of any program, it is important to pay close attention to accurately describing the information requested from the public, failing which it can be very time-consuming to select relevant data from the set of information received. It may also be the case that, due to the incorrect or unverifiable data received, the decision-making bodies may not take into account the results of such a project. It is particularly difficult to filter out or prevent the creation of such erroneous data, perhaps because citizen science is still often characterized by a lack of universal, reproducible methods. The introduction and strict adherence to these methods can easily dampen the enthusiasm of the participating civilians, which is why the high level of attention in project design is important (MacPhail & Colla, 2020).
The form of the requested data may also be crucial for the preparation of the research. In monitoring the distribution of tick species, where, for example, citizen scientists may try to identify an animal found, the participants have three ways to submit the requested information. They can only send the name of the species identified, the photographic documentation of the individual, or the specimen itself. All three options have advantages and disadvantages, the first case favours large amounts of incoming data, but there is no way to verify them. In the second case, a lot depends on whether the person making the shot is aware of what morphological characters make the identification possible, e.g., from what angle and at what resolution it is worth taking pictures. The exact identification is most secure when citizen scientists send the specimen to be identified by professionals. We advised the participants to do so, however, in addition to being the most time consuming, this case raises other issues. Submission might involve the destruction of the specimen, and on the other hand, it increases the risk of human-tick contact (Eisen & Eisen, n.d.). Therefore, we particularly made our participants aware of the risks and suggested the safe removal, storage and postage of tick specimens.
The most commonly submitted tick species was I. ricinus . This is in line with the widespread distribution of this species, however, it also shows that participants do frequently not recognise the most common tick species. Dermacentor ticks were also submitted in large numbers. This is again partly due to the common occurrence of this tick species throughout the country (G. Földvári et al., 2007), however the on-line media also biased the study in this aspect. Unfortunately, several news portals used images that featured a Dermacentorspecies instead of a Hyalomma tick. As a consequence, many citizen scientists, especially dog owners, sent Dermacentorspecimens that are larger and quicker compared to I. ricinus and, in addition, matched the mistakenly included photograph of some online portals. We archived all tick specimens and data for further analyses, thus this by-catch might provide important epidemiological data in the future.
Mitochondrial gene-based genetic analysis is highly important to reveal dispersal patterns and introduction routes of Hyalomma ticks (Capek et al., 2014; Wallménius et al., 2014). Novel mitochondrial sequence data for Hyalomma spp. is increasingly reported (Ciloglu et al., 2021; Lang, Shan, Zhang, Liu, & Wang, 2022). The importance of providing sequence data of these vector organisms is getting more relevant in the light of disease emergence, especially the geographic expansion of Crimean-Congo Haemorrhagic Fever virus during the last decades (Akyildiz, Bente, Keles, Vatansever, & Kar, 2021; Arteaga et al., 2021; Moraga-Fernández et al., 2021; Sánchez-Seco et al., n.d.). We further highlight the importance of sequence data by integrating this activity into the citizens science programme and also into the risk assessment of CCHFV emergence and preparedness in our region. The two sites were Hyalomma ticks were found in our study are approximately 280 kilometres apart, with the first specimen discovered on August 10 and the second on September 10, so exactly one month apart. Due to the large geographical distance and the time difference, the two specimens must have arrived in the country separately as a result of two separate introductions. Although much more published sequence data would be necessary, we suspect that the probable source of introduction was a Eurasian population for the detected Hy. marginatum and a population along the Africa-Europe bird migration route for Hy. rufipes .
Another important issue is whether the specimens found entered the country in the same year, e.g. as engorged nymphs dropping off from migratory birds, or overwintered before finding them in the next year, or even already hatched here as larvae in the previous year. The latter possibility is of greatest concern because it would indicate the establishment of a local population, making this species able to successfully complete its entire life cycle in Hungary. This seems unlikely currently, because a critical number of conspecificHyalomma adults would be needed to yield egg-laying fertilized females. The moulting into adult in the year of drop-off, among many other factors, is affected mainly by temperature. On the one hand, hot springs are preferred by Hyalomma ticks, where the average daily temperature above 8 ° C for Hy. marginatum ticks can be determined as a criterion for moulting from nymph to adult (Gale et al., 2012). Due to the colder-than-average April weather in Hungary in 2021, this was only achieved in mid-May (National Meteorological Service). Only adults found before this could have unambiguously overwintered in the country, giving the opportunity to develop a local population. However, during our program, both specimens of Hyalomma were discovered well after May, so these adults were presumably introduced the same year. Our tick monitoring program was not running during the spring, and there is a possibility for overwintering adultHyalomma in Hungary, as it has recently been shown in the Czech Republic (Rudolf et al., 2021). Unfed adult Hyalomma ticks tolerate the cold months well, with the most critical period being late summer and autumn due to the heat sensitivity of engorged nymphs (Uiterwijk et al., 2021; Valcárcel et al., 2020). Thus, it is not the cold winter but the cold autumn that is critical in shaping the geographical spread of Hyalomma species. Climate change might easily enhance establishment of new local Hyalomma populations with elevating autumn temperatures in temperate Europe as exemplified by the rising presence of the tick Hy. marginatum in Southern France (Vial et al., 2016). Once imported, establishment of Hy. marginatum on common local hosts, wild and domesticated mammals and even urban ones like hedgehog has been shown in Hungary (G Földvári et al., 2011) and also recently in Bulgaria (Arnaudov, Mikov, & Georgiev, 2022).
The ultimate reason for monitoring the emergence of adultHyalomma ticks is the possible introduction of tick-borne pathogens, most importantly Crimean-Congo Haemorrhagic Fever Virus. There are scattered historical data about the occurrence ofHyalomma ticks and CCHFV in Hungary as summarised in Figure 4. Immature Hy. marginatum from a hedgehog in a city park (G Földvári et al., 2011), immature Hy. rufipes and Hy. marginatum from songbirds (S Hornok et al., 2013; S. Hornok et al., 2016) and two adult Hy. rufipes from cattle were previously detected in the country. Reported occurrence of CCHFV spans from isolation from Ixodes ricinus ticks (Molnár, 1982), to seropositive cattle, sheep (S. Horváth, 1974), brown hares (Németh et al., 2013) and wild rodents (Földes et al., 2019). Most interestingly, humans seropositive for CCHFV were reported well before the first observation of adult Hyalomma ticks (L. B. Horváth, 1976). There was also a reported human case of CCHF with unknown origin in 2004 (Országos Epidemiológiai Központ, 2008) and CCHFV seropositives were detected in 12 healthy blood donors collected between 2008-2017 (Magyar et al., 2021). All these data indicate that CCHFV might be transmitted by tick species other than Hyalomma spp. and that the earlier emergence of adult Hyalomma ticks might have been overlooked in Hungary. In any case, we will continue with the citizen science based systematic monitoring of Hyalomma ticks in the future. We also plan to analyse these and future Hyalomma specimens for the occurrence of CCHFV and other pathogens.